Impact of assimilable nitrogen availability in glucose uptake kinetics in Saccharomyces cerevisiae during alcoholic fermentation

Microbial Cell Factories

Volumn 11, Issue , 2012, Pages

  Palma, Margarida ^a   Madeira, Sara C ^a,b   Mendes Ferreira, Ana ^c   Sá Correia, Isabel ^a  

^a INSTITUTO SUPERIOR TÉCNICO   (Portugal)

^b INESC ID   (Portugal)

^c UNIVERSITY OF TRÁS OS MONTES AND ALTO DOURO   (Portugal)

Author keywords

Alcoholic fermentation; Biclustering analysis; Glucose uptake kinetics; Hexose transporters; Nitrogen regulation; Yeast

Indexed keywords

AMMONIA; GLUCOSE; NITROGEN;

ALCOHOLIC FERMENTATION; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FERMENTATION; GENE EXPRESSION; GLUCOSE TRANSPORT; GRAPE JUICE; NITROGEN AVAILABILITY; NONHUMAN; SACCHAROMYCES CEREVISIAE;

ETHANOL; FERMENTATION; GLUCOSE; GLUCOSE TRANSPORT PROTEINS, FACILITATIVE; KINETICS; NITROGEN; QUATERNARY AMMONIUM COMPOUNDS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE; VITACEAE;

EID: 84864371726     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/1475-2859-11-99     Document Type: Article

References (46)

1. Graves T, Narendranath NV, Dawson K, Power R. Effect of pH and lactic or acetic acid on ethanol productivity by Saccharomyces cerevisiae in corn mash. J Ind Microbiol Biotechnol 2006, 33:469-474. 10.1007/s10295-006-0091-6, 16491359.
2. Garay-Arroyo A, Covarrubias AA, Clark I, Niño I, Gosset G, Martinez A. Response to different environmental stress conditions of industrial and laboratory Saccharomyces cerevisiae strains. Appl Microbiol Biotechnol 2004, 63:734-741. 10.1007/s00253-003-1414-4, 12910327.
3. Jackson RS. Wine Science. Principles and applications 2008, Academic Press, San Diego, 3.
4. Teixeira MC, Mira NP, Sá-Correia I. A genome-wide perspective on the response and tolerance to food-relevant stresses in Saccharomyces cerevisiae. Curr Opin Biotechnol 2011, 22:150-156. 10.1016/j.copbio.2010.10.011, 21087853.
5. Jeronimo EM, Oliveira ES, Rocha Souza EL, Silva MA, Serra GE. Addition of proteic nitrogen during alcoholic fermentation for the production of cachaça. Sci Agric 2008, 65:161-168.
6. O'Connor-Cox ESC, Paik J, Ingeldew WM. Improved ethanol yields through supplementation with excess assimilable nitrogen. J Ind Microbiol 1991, 8:45-52.
7. Thomas KC, Ingledew WM. Fuel alcohol production: effects of free amino nitrogen on fermentation of very-high-gravity wheat mashes. Appl Environ Microbiol 1990, 56:2046-2050. 184558, 2202254.
8. Bely M, Salmon JM, Barre P. Assimilable nitrogen addition and hexose transport system activity during enological fermentation. J Inst Brew 1994, 100:279-282.
9. Mauricio JC, Salmon JM. Apparent loss of sugar transport activity in Saccharomyces cerevisiae mainly account for maximum ethanol production during alcoholic fermentation. Biotechnol Lett 1992, 14:577-582.
10. Salmon JM. Effect of sugar transport inactivation in Saccharomyces cerevisiae on sluggish and stuck enological fermentations. Appl Environ Microbiol 1989, 55:953-958. 184230, 16347895.
11. Salmon JM, Vincent O, Mauricio JC, Bely M, Barre P. Sugar transport inhibition and apparent loss of activity in Saccharomyces cerevisiae as a major limiting factor of enological fermentation. Am J Enol Vitic 1993, 44:56-64.
12. Reifenberger E, Freidel K, Ciriacy M. Identification of novel HXT genes in Saccharomyces cerevisiae reveals the impact of individual hexose transporters on glycolytic flux. Mol Microbiol 1995, 16:157-167. 10.1111/j.1365-2958.1995.tb02400.x, 7651133.
13. Buziol S, Warth L, Magario I, Freund A, Siemann-Herzberg M, Reuss M. Dynamic response of the expression of hxt1, hxt5 and hxt7 transport proteins in Saccharomyces cerevisiae to perturbations in the extracellular glucose concentration. J Biotechnol 2008, 134:203-210. 10.1016/j.jbiotec.2008.02.002, 18367282.
14. Özcan S, Johnston M. Three different regulatory mechanisms enable yeast hexose transporter (HXT) genes to be induced by different levels of glucose. Mol Cell Biol 1995, 15:1564-1572. 230380, 7862149.
15. Liang H, Gaber RF. A novel signal transduction pathway in Saccharomyces cerevisiae defined by Snf3-regulated expression of HXT6. Mol Biol Cell 1996, 7:1953-1966. 276042, 8970157.
16. Ye L, Berden JA, van Dam K, Kruckeberg AL. Expression and activity of the Hxt7 high-affinity hexose transporter of Saccharomyces cerevisiae. Yeast 2001, 18:1257-1267. 10.1002/yea.771, 11561293.
17. Reifenberger E, Boles E, Ciriacy M. Kinetic characterization of individual hexose transporters of Saccharomyces cerevisiae and their relation to the triggering mechanisms of glucose repression. Eur J Biochem 1997, 245:324-333. 10.1111/j.1432-1033.1997.00324.x, 9151960.
18. Diderich JA, Schepper M, van Hoek P, Luttik MA, van Dijken JP, Pronk JT, Klaassen P, Boelens HF, de Mattos MJ, van Dam K, Kruckeberg AL. Glucose uptake kinetics and transcription of HXT genes in chemostat cultures of Saccharomyces cerevisiae. J Biol Chem 1999, 274:15350-15359. 10.1074/jbc.274.22.15350, 10336421.
19. Diderich JA, Schuurmans JM, Van Gaalen MC, Kruckeberg AL, Van Dam K. Functional analysis of the hexose transporter homologue HXT5 in Saccharomyces cerevisiae. Yeast 2001, 18:1515-1524. 10.1002/yea.779, 11748728.
20. Verwaal R, Paalman JWG, Hogenkamp A, Verkleij AJ, Verrips CT, Boonstra J. HXT5 expression is determined by growth rates in Saccharomyces cerevisiae. Yeast 2002, 19:1029-1038. 10.1002/yea.895, 12210898.
21. Buziol S, Becker J, Baumeister A, Jung S, Mauch K, Reuss M, Boles E. Determination of in vivo kinetics of the starvation-induced Hxt5 glucose transporter of Saccharomyces cerevisiae. FEMS Yeast Res 2002, 2:283-291.
22. Krampe S, Stamm O, Hollenberg CP, Boles E. Catabolite inactivation of the high-affinity hexose transporters Hxt6 and Hxt7 of Saccharomyces cerevisiae occurs in the vacuole after internalization by endocytosis. FEBS Lett 1998, 441:343-347. 10.1016/S0014-5793(98)01583-X, 9891967.
23. van Suylekom D, van Donselaar E, Blanchetot C, Do Ngoc LN, Humbel BM, Boonstra J. Degradation of the hexose transporter Hxt5p in Saccharomyces cerevisiae. Biol Cell 2007, 99:13-23. 10.1042/BC20060040, 16928197.
24. Kruckeberg AL, Ye L, Berden JA, van Dam K. Functional expression, quantification and cellular localization of the Hxt2 hexose transporter of Saccharomyces cerevisiae tagged with the green fluorescent protein. Biochem J 1999, 339:299-307. 10.1042/0264-6021:3390299, 1220158, 10191260.
25. Krampe S, Boles E. Starvation-induced degradation of yeast hexose transporter Hxt7p is dependent on endocytosis, autophagy and the terminal sequences of the permease. FEBS Lett 2002, 513:193-196. 10.1016/S0014-5793(02)02297-4, 11904149.
26. Mendes-Ferreira A, del Olmo M, Garcia-Martinez J, Jimenez-Marti E, Mendes-Faia A, Perez-Ortin JE, Leão C. Transcriptional response of Saccharomyces cerevisiae to different nitrogen concentrations during alcoholic fermentation. Appl Environ Microbiol 2007, 73:3049-3060. 10.1128/AEM.02754-06, 1892875, 17337556.
27. Madeira SC, Teixeira MC, Sa-Correia I, Oliveira AL. Identification of regulatory modules in time series gene expression data using a linear time biclustering algorithm. Trans Comput Biol Bioinform 2010, 7:153-165.
28. Mendes-Ferreira A, Mendes-Faia A, Leão C. Growth and fermentation patterns of Saccharomyces cerevisiae under different ammonium concentrations and its implications in winemaking industry. J Appl Microbiol 2004, 97:540-545. 10.1111/j.1365-2672.2004.02331.x, 15281934.
29. dos Santos SC, Tenreiro S, Palma M, Becker J, Sá-Correia I. Transcriptomic profiling of the Saccharomyces cerevisiae response to quinine reveals a glucose limitation response attributable to drug-induced inhibition of glucose uptake. Antimicrob Agents Chemother 2009, 53:5213-5223. 10.1128/AAC.00794-09, 2786357, 19805573.
30. Walsh MC, Smits HP, Scholte M, van Dam K. Affinity of glucose transport in Saccharomyces cerevisiae is modulated during growth on glucose. J Bacteriol 1994, 176:953-958. 205144, 8106337.
31. Coons DM, Boulton RB, Bisson LF. Computer-assisted nonlinear regression analysis of the multicomponent glucose uptake kinetics of Saccharomyces cerevisiae. J Bacteriol 1995, 177:3251-3258. 177018, 7768825.
32. Maier A, Volker B, Boles E, Fuhrmann GF. Characterisation of glucose transport in Saccharomyces cerevisiae with plasma membrane vesicles (countertransport) and intact cells (initial uptake) with single Hxt1, Hxt2, Hxt3, Hxt4, Hxt6, Hxt7 or Gal2 transporters. FEMS Yeast Res 2002, 2:539-550.
33. Perez M, Luyten K, Michel R, Riou C, Blondin B. Analysis of Saccharomyces cerevisiae hexose carrier expression during wine fermentation: both low- and high-affinity Hxt transporters are expressed. FEMS Yeast Res 2005, 5:351-361. 10.1016/j.femsyr.2004.09.005, 15691740.
34. Teixeira MC, Monteiro P, Jain P, Tenreiro S, Fernandes AR, Mira NP, Alenquer M, Freitas AT, Oliveira AL, Sá-Correia I. The YEASTRACT database: a tool for the analysis of transcription regulatory associations in Saccharomyces cerevisiae. Nucleic Acids Res 2006, 34:D446-D451. 10.1093/nar/gkj013, 1347376, 16381908.
35. Georis I, Feller A, Vierendeels F, Dubois E. The yeast GATA factor Gat1 occupies a central position in nitrogen catabolite repression-sensitive gene activation. Mol Cell Biol 2009, 29:3803-3815. 10.1128/MCB.00399-09, 2698774, 19380492.
36. Zhang N, Wu J, Oliver SG. Gis1 is required for transcriptional reprogramming of carbon metabolism and the stress response during transition into stationary phase in yeast. Microbiology 2009, 155:1690-1698. 10.1099/mic.0.026377-0, 19383711.
37. Lai LC, Kosorukoff AL, Burke PV, Kwast KE. Dynamical remodeling of the transcriptome during short-term anaerobiosis in Saccharomyces cerevisiae: differential response and role of Msn2 and/or Msn4 and other factors in galactose and glucose media. Mol Cell Biol 2005, 25:4075-4091. 10.1128/MCB.25.10.4075-4091.2005, 1087712, 15870279.
38. Verwaal R, Arako M, Kapur R, Verkleij AJ, Verrips CT, Boonstra J. HXT5 expression is under control of STRE and HAP elements in the HXT5 promoter. Yeast 2004, 21:747-757. 10.1002/yea.1106, 15282798.
39. Tomas-Cobos L, Casadome L, Mas G, Sanz P, Posas F. Expression of the HXT1 low affinity glucose transporter requires the coordinated activities of the HOG and glucose signalling pathways. J Biol Chem 2004, 279:22010-22019. 10.1074/jbc.M400609200, 15014083.
40. Tomas-Cobos L, Viana R, Sanz P. TOR kinase pathway and 14-3-3 proteins regulate glucose-induced expression of HXT1, a yeast low-affinity glucose transporter. Yeast 2005, 22:471-479. 10.1002/yea.1224, 15849787.
41. Schmelzle T, Beck T, Martin DE, Hall MN. Activation of the RAS/cyclic AMP pathway suppresses a TOR deficiency in yeast. Mol Cell Biol 2004, 24:338-351. 10.1128/MCB.24.1.338-351.2004, 303340, 14673167.
42. Karpel JE, Place WR, Bisson LF. Analysis of the Major Hexose Transporter Genes in Wine Strains of Saccharomyces cerevisiae. Am J Enol Vitic 2008, 59:265-275.
43. Monteiro GA, Sá-Correia I. In vivo activation of yeast plasma membrane H + -ATPase by ethanol: effect on the kinetic parameters and involvement of the carboxyl-terminus regulatory domain. Biochim Biophys Acta 1998, 1370:310-316. 10.1016/S0005-2736(97)00281-2, 9545589.
44. Rosa MF, Sá-Correia I. In vivo activation by ethanol of plasma membrane ATPase of Saccharomyces cerevisiae. Appl Environ Microbiol 1991, 57:830-835. 182802, 1645512.
45. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO. Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 2000, 11:4241-4257. 15070, 11102521.
46. Marks VD, Ho Sui SJ, Erasmus D, van der Merwe GK, Brumm J, Wasserman WW, Bryan J, van Vuuren HJ. Dynamics of the yeast transcriptome during wine fermentation reveals a novel fermentation stress response. FEMS Yeast Res 2008, 8:35-52. 10.1111/j.1567-1364.2007.00338.x, 18215224.